Blindness affects the developmental trajectory of the sleeping brain.

Sleep plays a crucial role in brain development, sensory information processing, and consolidation. Sleep spindles are markers of these mechanisms as they mirror the activity of the thalamocortical circuits. Spindles can be subdivided into two groups, slow (10-13 Hz) and fast (13-16 Hz), which are each associated with different functions. Specifically, fast spindles oscillate in the high-sigma band and are associated with sensorimotor processing, which is affected by visual deprivation. However, how blindness influences spindle development has not yet been investigated. We recorded nap video-EEG of 50 blind/severely visually impaired (BSI) and 64 sighted children aged 5 months to 6 years old. We considered aspects of both macro- and micro-structural spindles. The BSI children lacked the evolution of developmental spindles within the central area. Specifically, young BSI children presented low central high-sigma and high-beta (25-30 Hz) event-related spectral perturbation and showed no signs of maturational decrease. High-sigma and high-beta activity in the BSI group correlated with clinical indices predicting perceptual and motor disorders. Our findings suggest that fast spindles are pivotal biomarkers for identifying an early developmental deviation in BSI children. These findings are critical for initial therapeutic intervention.

The effect of visuo-haptic exploration on the development of the geometric cross-sectioning ability.

Cross-sectioning is a shape understanding task where the participants must infer and interpret the spatial features of three-dimensional (3D) solids by depicting their internal two-dimensional (2D) arrangement. An increasing body of research provides evidence of the crucial role of sensorimotor experience in acquiring these complex geometrical concepts. Here, we focused on how cross-sectioning ability emerges in young children and the influence of multisensory visuo-haptic experience in geometrical learning through two experiments. In Experiment 1, we compared the 3D printed version of the Santa Barbara Solids Test (SBST) with its classical paper version; in Experiment 2, we contrasted the children's performance in the SBST before and after the visual or visuo-haptic experience. In Experiment 1, we did not identify an advantage in visualizing 3D shapes over the classical 2D paper test. In contrast, in Experiment 2, we found that children who had the experience of a combination of visual and tactile information during the exploration phase improved their performance in the SBST compared with children who were limited to visual exploration. Our study demonstrates how practicing novel multisensory strategies improves children's understanding of complex geometrical concepts. This outcome highlights the importance of introducing multisensory experience in educational training and the need to make way for developing new technologies that could improve learning abilities in children.

Vestibular contribution to spatial encoding.

Determining the spatial relation between objects and our location in the surroundings is essential for survival. Vestibular inputs provide key information about the position and movement of our head in the three-dimensional space, contributing to spatial navigation. Yet, their role in encoding spatial localisation of environmental targets remains to be fully understood. We probed the accuracy and precision of healthy participants' representations of environmental space by measuring their ability to encode the spatial location of visual targets (Experiment 1). Participants were asked to detect a visual light and then walk towards it. Vestibular signalling was artificially disrupted using stochastic galvanic vestibular stimulation (sGVS) applied selectively during encoding targets' location. sGVS impaired the accuracy and precision of locating the environmental visual targets. Importantly, this effect was specific to the visual modality. The location of acoustic targets was not influenced by vestibular alterations (Experiment 2). Our findings indicate that the vestibular system plays a role in localising visual targets in the surrounding environment, suggesting a crucial functional interaction between vestibular and visual signals for the encoding of the spatial relationship between our body position and the surrounding objects.

Multisensory representations of space and time in sensory cortices.

Clear evidence demonstrated a supramodal organization of sensory cortices with multisensory processing occurring even at early stages of information encoding. Within this context, early recruitment of sensory areas is necessary for the development of fine domain-specific (i.e., spatial or temporal) skills regardless of the sensory modality involved, with auditory areas playing a crucial role in temporal processing and visual areas in spatial processing. Given the domain-specificity and the multisensory nature of sensory areas, in this study, we hypothesized that preferential domains of representation (i.e., space and time) of visual and auditory cortices are also evident in the early processing of multisensory information. Thus, we measured the event-related potential (ERP) responses of 16 participants while performing multisensory spatial and temporal bisection tasks. Audiovisual stimuli occurred at three different spatial positions and time lags and participants had to evaluate whether the second stimulus was spatially (spatial bisection task) or temporally (temporal bisection task) farther from the first or third audiovisual stimulus. As predicted, the second audiovisual stimulus of both spatial and temporal bisection tasks elicited an early ERP response (time window 50-90 ms) in visual and auditory regions. However, this early ERP component was more substantial in the occipital areas during the spatial bisection task, and in the temporal regions during the temporal bisection task. Overall, these results confirmed the domain specificity of visual and auditory cortices and revealed that this aspect selectively modulates also the cortical activity in response to multisensory stimuli.

The Suite for the Assessment of Low-Level cues on Orientation (SALLO): The psychophysics of spatial orientation in virtual reality.

Spatial orientation is a complex ability that emerges from the interaction of several systems in a way that is still unclear. One of the reasons limiting the research on the topic is the lack of methodologies aimed at studying multimodal psychophysics in an ecological manner and with affordable settings. Virtual reality can provide a workaround to this impasse by using virtual stimuli rather than real ones. However, the available virtual reality development platforms are not meant for psychophysical testing; therefore, using them as such can be very difficult for newcomers, especially the ones new to coding. For this reason, we developed SALLO, the Suite for the Assessment of Low-Level cues on Orientation, which is a suite of utilities that simplifies assessing the psychophysics of multimodal spatial orientation in virtual reality. The tools in it cover all the fundamental steps to design a psychophysical experiment. Plus, dedicated tracks guide the users in extending the suite components to simplify developing new experiments. An experimental use-case used SALLO and virtual reality to show that the head posture affects both the egocentric and the allocentric mental representations of spatial orientation. Such a use-case demonstrated how SALLO and virtual reality can be used to accelerate hypothesis testing concerning the psychophysics of spatial orientation and, more broadly, how the community of researchers in the field may benefit from such a tool to carry out their investigations.

The power of vision: calibration of auditory space after sight restoration from congenital cataracts.

Early visual deprivation typically results in spatial impairments in other sensory modalities. It has been suggested that, since vision provides the most accurate spatial information, it is used for calibrating space in the other senses. Here we investigated whether sight restoration after prolonged early onset visual impairment can lead to the development of more accurate auditory space perception. We tested participants who were surgically treated for congenital dense bilateral cataracts several years after birth. In Experiment 1 we assessed participants' ability to understand spatial relationships among sounds, by asking them to spatially bisect three consecutive, laterally separated sounds. Participants performed better after surgery than participants tested before. However, they still performed worse than sighted controls. In Experiment 2, we demonstrated that single sound localization in the two-dimensional frontal plane improves quickly after surgery, approaching performance levels of sighted controls. Such recovery seems to be mediated by visual acuity, as participants gaining higher post-surgical visual acuity performed better in both experiments. These findings provide strong support for the hypothesis that vision calibrates auditory space perception. Importantly, this also demonstrates that this process can occur even when vision is restored after years of visual deprivation.

Different mechanisms of magnitude and spatial representation for tactile and auditory modalities.

The human brain creates an external world representation based on magnitude judgments by estimating distance, numerosity, or size. The magnitude and spatial representation are hypothesized to rely on common mechanisms shared by different sensory modalities. We explored the relationship between magnitude and spatial representation using two different sensory systems. We hypothesize that the interaction between space and magnitude is combined differently depending on sensory modalities. Furthermore, we aimed to understand the role of the spatial reference frame in magnitude representation. We used stimulus-response compatibility (SRC) to investigate these processes assuming that performance is improved if stimulus and response share common features. We designed an auditory and tactile SRC task with conflicting spatial and magnitude mapping. Our results showed that sensory modality modulates the relationship between space and magnitude. A larger effect of magnitude over spatial congruency occurred in a tactile task. However, magnitude and space showed similar weight in the auditory task, with neither spatial congruency nor magnitude congruency having a significant effect. Moreover, we observed that the spatial frame activated during tasks was elicited by the sensory inputs. The participants' performance was reversed in the tactile task between uncrossed and crossed hands posture, suggesting an internal coordinate system. In contrast, crossing the hands did not alter performance (i.e., using an allocentric frame of reference). Overall, these results suggest that space and magnitude interaction differ in auditory and tactile modalities, supporting the idea that these sensory modalities use different magnitude and spatial representation mechanisms.

Balance, gait, and navigation performance are related to physical exercise in blind and visually impaired children and adolescents.

Self-motion perception used for locomotion and navigation requires the integration of visual, vestibular, and proprioceptive input. In the absence of vision, postural stability and locomotor tasks become more difficult. Previous research has suggested that in visually deprived children, postural stability and levels of physical activity are overall lower than in sighted controls. Here we hypothesized that visually impaired and blind children and adolescents differ from sighted controls in postural stability and gait parameters, and that physically active individuals outperform sedentary peers in postural stability and gait parameters as well as in navigation performance. Fourteen blind and visually impaired children and adolescents (8-18 years of age) and 14 matched sighted individuals took part. Assessments included postural sway, single-leg stance time, parameters of gait variability and stability, self-reported physical activity, and navigation performance. Postural sway was larger and single-leg stance time was lower in blind and visually impaired participants than in blindfolded sighted individuals. Physical activity was higher in the sighted group. No differences between the group of blind and visually impaired and blindfolded sighted participants were observed for gait parameters and navigation performance. Higher levels of physical activity were related to lower postural sway, longer single-leg stance time, higher gait stability, and superior navigation performance in blind and visually impaired participants. The present data suggest that physical activity may enhance postural stability and gait parameters, and thereby promote navigation performance in blind and visually impaired children and adolescents.

The development of allocentric spatial frame in the auditory system.

The ability to encode space is a crucial aspect of interacting with the external world. Therefore, this ability appears to be fundamental for the correct development of the capacity to integrate different spatial reference frames. The spatial reference frame seems to be present in all the sensory modalities. However, it has been demonstrated that different sensory modalities follow various developmental courses. Nevertheless, to date these courses have been investigated only in people with sensory impairments, where there is a possible bias due to compensatory strategies and it is complicated to assess the exact age when these skills emerge. For these reasons, we investigated the development of the allocentric frame in the auditory domain in a group of typically developing children aged 6-10 years. To do so, we used an auditory Simon task, a paradigm that involves implicit spatial processing, and we asked children to perform the task in both the uncrossed and crossed hands postures. We demonstrated that the crossed hands posture affected the performance only in younger children (6-7 years), whereas at 10 years of age children performed as adults and were not affected by such posture. Moreover, we found that this task's performance correlated with age and developmental differences in spatial abilities. Our results support the hypothesis that auditory spatial cognition's developmental course is similar to the visual modality development as reported in the literature.

Allocentric spatial perception through vision and touch in sighted and blind children.

Vision and touch play a critical role in spatial development, facilitating the acquisition of allocentric and egocentric frames of reference, respectively. Previous works have shown that children's ability to adopt an allocentric frame of reference might be impaired by the absence of visual experience during growth. In the current work, we investigated whether visual deprivation also impairs the ability to shift from egocentric to allocentric frames of reference in a switching-perspective task performed in the visual and haptic domains. Children with and without visual impairments from 6 to 13 years of age were asked to visually (only sighted children) or haptically (blindfolded sighted children and blind children) explore and reproduce a spatial configuration of coins by assuming either an egocentric perspective or an allocentric perspective. Results indicated that temporary visual deprivation impaired the ability of blindfolded sighted children to switch from egocentric to allocentric perspective more in the haptic domain than in the visual domain. Moreover, results on visually impaired children indicated that blindness did not impair allocentric spatial coding in the haptic domain but rather affected the ability to rely on haptic egocentric cues in the switching-perspective task. Finally, our findings suggested that the total absence of vision might impair the development of an egocentric perspective in case of body midline-crossing targets.

Factors Affecting Auditory Estimates of Virtual Room Size: Effects of Stimulus, Level, and Reverberation.

When vision is unavailable, auditory level and reverberation cues provide important spatial information regarding the environment, such as the size of a room. We investigated how room-size estimates were affected by stimulus type, level, and reverberation. In Experiment 1, 15 blindfolded participants estimated room size after performing a distance bisection task in virtual rooms that were either anechoic (with level cues only) or reverberant (with level and reverberation cues) with a relatively short reverberation time of T60 = 400 milliseconds. Speech, noise, or clicks were presented at distances between 1.9 and 7.1 m. The reverberant room was judged to be significantly larger than the anechoic room (p < .05) for all stimuli. In Experiment 2, only the reverberant room was used and the overall level of all sounds was equalized, so only reverberation cues were available. Ten blindfolded participants took part. Room-size estimates were significantly larger for speech than for clicks or noise. The results show that when level and reverberation cues are present, reverberation increases judged room size. Even relatively weak reverberation cues provide room-size information, which could potentially be used by blind or visually impaired individuals encountering novel rooms.

Visual representations of time elicit early responses in human temporal cortex.

Time perception is inherently part of human life. All human sensory modalities are always involved in the complex task of creating a temporal representation of the external world. However, when representing time, people primarily rely on auditory information. Since the auditory system prevails in many audio-visual temporal tasks, one may expect that the early recruitment of the auditory network is necessary for building a highly resolved and flexible temporal representation in the visual modality. To test this hypothesis, we asked 17 healthy participants to temporally bisect three consecutive flashes while we recorded EEG. We demonstrated that visual stimuli during temporal bisection elicit an early (50-90 â€‹ms) response of an extended area of the temporal cortex, likely including auditory cortex too. The same activation did not appear during an easier spatial bisection task. These findings suggest that the brain may use auditory representations to deal with complex temporal representation in the visual system.

Temporal cues trick the visual and auditory cortices mimicking spatial cues in blind individuals.

In the absence of vision, spatial representation may be altered. When asked to compare the relative distances between three sounds (i.e., auditory spatial bisection task), blind individuals demonstrate significant deficits and do not show an event-related potential response mimicking the visual C1 reported in sighted people. However, we have recently demonstrated that the spatial deficit disappears if coherent time and space cues are presented to blind people, suggesting that they may use time information to infer spatial maps. In this study, we examined whether the modification of temporal cues during space evaluation altered the recruitment of the visual and auditory cortices in blind individuals. We demonstrated that the early (50-90 ms) occipital response, mimicking the visual C1, is not elicited by the physical position of the sound, but by its virtual position suggested by its temporal delay. Even more impressively, in the same time window, the auditory cortex also showed this pattern and responded to temporal instead of spatial coordinates.

Children can optimally integrate multisensory information after a short action-like mini game training.

Combining information across different sensory modalities is of critical importance for the animal's survival and a core feature of human's everyday life. In adulthood, sensory information is often integrated in a statistically optimal fashion, so that the combined estimates of two or more senses are more reliable than the best single one. Several studies have shown that young children use one sense to calibrate the others, which results in unisensory dominance and undermines their optimal multisensory integration abilities. In this study we trained children aged 4-5 years with action-like mini games, to determine whether it could improve their multisensory as well as their visuo-spatial skills. Multisensory integration abilities were assessed using a visuo-haptic size discrimination task, while visuo-spatial attention skills were investigated using a multiple object tracking task (MOT). We found that 2-weeks training were sufficient to observe both optimal multisensory integration and visuo-spatial enhancements selectively in the group trained with action-like mini games. This plastic change persisted up to 3 months, as assessed in a follow-up. Our novel findings reveal that abilities that are commonly known to emerge in late childhood can be promoted in younger children through action-like mini games and have long-lasting effects. Our data have clinical implications, in that they suggest that specific trainings could potentially help children with multisensory integration deficits.

Temporal representation impairment in developmental dyslexia for unisensory and multisensory stimuli.

Dyslexia has been associated with a problem in visual-audio integration mechanisms. Here, we investigate for the first time the contribution of unisensory cues on multisensory audio and visual integration in 32 dyslexic children by modelling results using the Bayesian approach. Non-linguistic stimuli were used. Children performed a temporal task: they had to report whether the middle of three stimuli was closer in time to the first one or to the last one presented. Children with dyslexia, compared with typical children, exhibited poorer unimodal thresholds, requiring greater temporal distance between items for correct judgements, while multisensory thresholds were well predicted by the Bayesian model. This result suggests that the multisensory deficit in dyslexia is due to impaired audio and visual inputs rather than impaired multisensory processing per se. We also observed that poorer temporal skills correlated with lower reading skills in dyslexic children, suggesting that this temporal capability can be linked to reading abilities.

Impact of years of blindness on neural circuits underlying auditory spatial representation.

Early visual deprivation impacts negatively on spatial bisection abilities. Recently, an early (50-90 ms) ERP response, selective for sound position in space, has been observed in the visual cortex of sighted individuals during the spatial but not the temporal bisection task. Here, we clarify the role of vision on spatial bisection abilities and neural correlates by studying late blind individuals. Results highlight that a shorter period of blindness is linked to a stronger contralateral activation in the visual cortex and a better performance during the spatial bisection task. Contrarily, not lateralized visual activation and lower performance are observed in individuals with a longer period of blindness. To conclude, the amount of time spent without vision may gradually impact on neural circuits underlying the construction of spatial representations in late blind participants. These findings suggest a key relationship between visual deprivation and auditory spatial abilities in humans.

Enhanced audio-tactile multisensory interaction in a peripersonal task after echolocation.

Peripersonal space (PPS) is created by a multisensory interaction between different sensory modalities and can be modified by experience. In this article, we investigated whether an auditory training, inside the peripersonal space area, can modify the PPS around the head in sighted participants. The auditory training was based on echolocation. We measured the participant's reaction times to a tactile stimulation on the neck, while task-irrelevant looming auditory stimuli were presented. Sounds more strongly affect tactile processing when located within a limited distance from the body. We measured spatially dependent audio-tactile interaction as a proxy of PPS representation before and after an echolocation training. We found a significant speeding effect on tactile RTs after echolocation, specifically when sounds where around the location where the echolocation task was performed. This effect could not be attributed to a task repetition effect nor to a shift of spatial attention, as no changes of PPS were found in two control groups of participants, who performed the PPS task after either a break or a temporal auditory task (with stimuli located at the same position of echolocation task). These findings show that echolocation affects multisensory processing inside PPS representation, likely to better represent the space where external stimuli, have to be localized.

Auditory and proprioceptive spatial impairments in blind children and adults.

It is not clear what role visual information plays in the development of space perception. It has previously been shown that in absence of vision, both the ability to judge orientation in the haptic modality and bisect intervals in the auditory modality are severely compromised (Gori, Sandini, Martinoli & Burr, 2010; Gori, Sandini, Martinoli & Burr, 2014). Here we report for the first time also a strong deficit in proprioceptive reproduction and audio distance evaluation in early blind children and adults. Interestingly, the deficit is not present in a small group of adults with acquired visual disability. Our results support the idea that in absence of vision the audio and proprioceptive spatial representations may be delayed or drastically weakened due to the lack of visual calibration over the auditory and haptic modalities during the critical period of development.

Motor commands induce time compression for tactile stimuli.

Saccades cause compression of visual space around the saccadic target, and also a compression of time, both phenomena thought to be related to the problem of maintaining saccadic stability (Morrone et al., 2005; Burr and Morrone, 2011). Interestingly, similar phenomena occur at the time of hand movements, when tactile stimuli are systematically mislocalized in the direction of the movement (Dassonville, 1995; Watanabe et al., 2009). In this study, we measured whether hand movements also cause an alteration of the perceived timing of tactile signals. Human participants compared the temporal separation between two pairs of tactile taps while moving their right hand in response to an auditory cue. The first pair of tactile taps was presented at variable times with respect to movement with a fixed onset asynchrony of 150 ms. Two seconds after test presentation, when the hand was stationary, the second pair of taps was delivered with a variable temporal separation. Tactile stimuli could be delivered to either the right moving or left stationary hand. When the tactile stimuli were presented to the motor effector just before and during movement, their perceived temporal separation was reduced. The time compression was effector-specific, as perceived time was veridical for the left stationary hand. The results indicate that time intervals are compressed around the time of hand movements. As for vision, the mislocalizations of time and space for touch stimuli may be consequences of a mechanism attempting to achieve perceptual stability during tactile exploration of objects, suggesting common strategies within different sensorimotor systems.

Children do not recalibrate motor-sensory temporal order after exposure to delayed sensory feedback.

Prolonged adaptation to delayed sensory feedback to a simple motor act (such as pressing a key) causes recalibration of sensory-motor synchronization, so instantaneous feedback appears to precede the motor act that caused it (Stetson, Cui, Montague & Eagleman, 2006). We investigated whether similar recalibration occurs in school-age children. Although plasticity may be expected to be even greater in children than in adults, we found no evidence of recalibration in children aged 8-11 years. Subjects adapted to delayed feedback for 100 trials, intermittently pressing a key that caused a tone to sound after a 200 ms delay. During the test phase, subjects responded to a visual cue by pressing a key, which triggered a tone to be played at variable intervals before or after the keypress. Subjects judged whether the tone preceded or followed the keypress, yielding psychometric functions estimating the delay when they perceived the tone to be synchronous with the action. The psychometric functions also gave an estimate of the precision of the temporal order judgment. In agreement with previous studies, adaptation caused a shift in perceived synchrony in adults, so the keypress appeared to trail behind the auditory feedback, implying sensory-motor recalibration. However, school children of 8 to 11 years showed no measureable adaptation of perceived simultaneity, even after adaptation with 500 ms lags. Importantly, precision in the simultaneity task also improved with age, and this developmental trend correlated strongly with the magnitude of recalibration. This suggests that lack of recalibration of sensory-motor simultaneity after adaptation in school-age children is related to their poor precision in temporal order judgments. To test this idea we measured recalibration in adult subjects with auditory noise added to the stimuli (which hampered temporal precision). Under these conditions, recalibration was greatly reduced, with the magnitude of recalibration strongly correlating with temporal precision.